Tensegrity: The architectural basis of cellular mechanotransduction

Annual Review of Physiology

Volumn 59, Issue , 1997, Pages 575-599

  Ingber, D E ^a  

^a BOSTON CHILDREN S HOSPITAL   (United States)

Author keywords

cytoskeleton; extracellular matrix; integrins; mechanoreceptor; signal transduction

Indexed keywords

ION CHANNEL;

CELL KINETICS; FORCE; HUMAN; HUMAN CELL; MECHANORECEPTOR; MOLECULAR BIOLOGY; PREDICTION; PRIORITY JOURNAL; REGULATORY MECHANISM; REVIEW; THERMODYNAMICS;

NASA DISCIPLINE CELL BIOLOGY; NON-NASA CENTER;

ANIMALS; HUMANS; KINETICS; MECHANORECEPTORS; MODELS, BIOLOGICAL; SIGNAL TRANSDUCTION; THERMODYNAMICS;

EID: 0030899760     PISSN: 00664278     EISSN: None     Source Type: Book Series    
DOI: 10.1146/annurev.physiol.59.1.575     Document Type: Review

References (80)

1. Albelda AM, Buck CA. 1990. Integrins and other cell adhesion molecules. FASEB J. 4:2868-80
2. Alon R, Hammer DA, Springer TA. 1995. Lifetime of the P-selectin-carbohydrate bond and its response to tensile force in hydrodynamic flow. Nature 374:539-42
3. Basdra EK, Papavassiliou AG, Huber LA. 1995. Rab and rho GTPases are involved in specific response of periodontal ligament fibroblasts to mechanical stretching. Biochim. Biophys. Acta 1268:209-13
4. Bassell GJ, Powers CM, Taneja KL, Singer RH. 1994. Single mRNAs visualized by ultrastructural in situ hybridization are principally localized at actin filament intersections in fibroblasts. J. Cell Biol. 126:863-76
5. Bershadsky AD, Tint IS, Svitkina TM. 1987. Association of intermediate filaments with vinculin-containing adhesion plaques of fibroblasts. Cell Motil. Cytoskelet. 8:274-83
6. Buxbaum RE, Heideman SR. 1988. A thermodynamic model for force integration and microtubule assembly during axonal elongation. J. Theor. Biol. 134:379-90
7. Chen BM, Grinnell AD. 1995. Integrins and modulation of transmitter release from motor nerve terminals by stretch. Science 269:1578-80
8. Davies PF. Flow-mediated endothelial mechanotransduction. Physiol. Rev. 75:519-60
9. Davies PF, Robotewsky JA, Griem ML. 1994. Quantitative studies of endothelial cell adhesion. Directional remodeling of focal adhesion sites in response to flow forces. J. Clin. Invest. 93:2031-38
10. Dennerll TJ, Joshi HC, Steel VL, Buxbaum RE, Heideman SR. 1988. Tension and compression in the cytoskeleton of PC-12 neuntes H: quantitative measurements. J. Cell Biol. 107:665-74
11. Ding JP, Pickard BG. 1993. Mechanosensory calcium-selective cation channels in epidermal cells. Plant J. 3:83-110
12. Du H, Gu G, William CM, Chalfie M. 1996 Extracellular proteins needed for C. elegans mechanosensation. Neuron 16:183-94
13. Duncan RL, Turner CH. 1995. Mechanotransduction and the functional response of bone to mechanical strain. Calcif. Tissue Int. 57:344-58
14. Ezzell RM, Goldmann WH, Wang N, Parasharama N, Ingber DE. 1996. Vinculin promotes cell spreading by mechanically coupling integrins to the cytoskeleton. J. Cell Biol. Submitted
15. Feldherr CM, Akin D. 1993. Regulation of nuclear transport in proliferating and quiescent cells. Exp. Cell Res. 205:179-86
16. French AS. 1992. Mechanotransduction. Annu. Rev. Physiol. 54:135-52
17. Fung YC. 1988. Biomechanics: Mechanical Properties of Living Tissues. New York: Springer-Verlag
18. Geiger B, Yehuda-Levenberg S, Bershadsky AD. 1996. Molecular interactions in the submembrane plaque of cell-cell and cell-matrix adhesions. Ann. Anat. In press
19. Gumbiner BM. 1993. Proteins associated with the cytoplasmic surface of adhesion molecules. Neuron 11:551-64
20. Hackney CM, Furness DN. 1995. Mechanotransduction invertebrate hair cells: structure and function of the stereociliary bundle. Am. J. Physiol. 268:C1-13
21. FAK. Biochem. Biophys. Res. Commun. 212:544-49
22. Harris AK, Wild P, Stopak D. 1980. Silicone rubber substrata: a new wrinkle in the study of cell locomotion. Science 208:177-80
23. Hamill OP, McBride DW Jr. 1992. Rapid adaptation of single mechanosensitive channels in Xenopus oocytes. Proc. Natl. Acad. Sci. USA 89:7462-66
24. He Y, Grinnell F. 1994. Stress relaxation of fibroblasts activates a cyclic AMP signaling pathway. J. Cell Biol. 126:457-64
25. Hill TL. 1981. Microfilament and microtubule assembly or disassociation against a force. Proc. Natl. Acad. Sci. USA 78:5613-17
26. Hong K, Driscoll M. 1994. A transmembrane domain of the putative channel subunit MEC-4 influences mechanotransduction and neurodegeneration in C. elegans. Nature 367:470-73
27. Ingber DE. 1991. Integrins as mechanochemical transducers. Curr. Opin. Cell Biol. 3:841-48
28. Ingber DE. 1993. Cellular tensegrity: defining new rules of biological design that govern the cytoskeleton. J. Cell Sci. 104:613-27
29. Ingber DE. 1993. The riddle of morphogenesis: a question of solution chemistry or molecular cell engineering? Cell 75:1249-52
30. Ingber DE. 1997. The architecture of life. Sci. Am. In press
31. Ingber DE, Dike L, Hansen L, Karp S, Liley H, et al. 1994. Cellular tensegrity. exploring how mechanical changes in the cytoskeleton regulate cell growth, migration, and tissue pattern during morphogenesis. Int. Rev. Cytol. 150:173-224
32. Ingber DE, Folkman J. 1989. Mechanochemical switching between growth and differentiation during fibroblast growth factor-stimulated angiogenesis in vitro: role of extracellular matrix. J. Cell biol. 109:317-30
33. Ingber DE, Folkman J. 1989. How does extracellular matrix control capillary morphogenesis? Cell 58:803-5
34. Ingber DE, Jamieson JD. 1985. Cells as tensegrity structures: architectural regulation of histodifferentiation by physical forces tranduced over basement membrane. In Gene Expression During Normal and Malignant Differentiation, ed. LC Andersson, CG Gahmberg, P Ekblom, pp. 13-32. Orlando, FL: Academic
35. Ingber DE, Madri JA, Folkman J. 1987. Extracellular matrix regulates endothelial growth factor action through modulation of cell and nuclear expansion. In Vitro Cell Dev. Biol. 23:387-94
36. Ingber DE, Madri JA, Jamieson JD. 1986. Basement membrane as a spatial organizer of polarized epithelia: Exogenous basement membrane reorients pancreatic epithelial tumor cells in vitro. Am. J. Pathol. 122:129-39
37. Ingber DE, Prusty D, Sun Z, Betensky H, Wang N. 1995. Cell shape, cytoskeletal mechanics and cell cycle control in angiogenesis. J. BioMechanics 28:1471-84
38. Joshi HC, Chu D, Buxbaum RE, Heideman SR. 1985. Tension and compression in the cytoskeleton of PC 12 neurites. J. Cell Biol. 101:697-705
39. Keller TC III. 1995. Structure and function of titin and nebulin. Curr. Opin. Cell Biol. 7:32-38
40. Kieffer JD, Plopper G, Ingber DE, Hartwig JH, Kupper TS. 1995. Direct binding of F-actin to the cytoplasmic domain of the α2 integrin chain in vitro. Biochem. Biophys. Res. Comm. 217:466-74
41. Kirschner M, Mitchison T. 1986. Beyond self-assembly: from microtubules to morphogenesis. Cell 45:329-42
42. Kolodnoy M, Wysolmerski RB. 1992. Isometric contraction by fibroblasts and endothelial cells in tissue culture: a quantitative study. J. Cell Biol. 117:73-82
43. Kuchan MJ, Jo H, Frangos JA. 1994. Role of G proteins in shear stress-mediated nitric oxide production by endothelial cells. Am. J. Physiol. 267:C753-58
44. Lamoureux P, Steel VL, Regal C, Adgate L, Buxbaum RE, Heideman SR. 1990. Extracellular matrix allows PC-12 neurite elongation in the absence of microtubules. J. Cell Biol. 110:71-79
45. Lauffenburger DA, Linderman JJ. 1993. Receptors: Models for Binding, Trafficking, and Signaling. New York: Oxford Univ. Press.
46. Malek AM, Izumo S. 1996. Mechanism of endothelial cell shape change and cytoskeletal remodeling in response to fluid shear stress. J. Cell Sci. 109:713-26
47. Manie S, Schmid-Alliana A, Kubar J, Ferrua B, Rossi B. 1993. Disruption of microtubule network in human monocytes induces expression of interleukin-1 but not that of interleukin-6 nor tumor necrosis factor-alpha. Involvement of protein kinase A stimulation. J. Biol. Chem. 268:13675-81
48. Maniotis A, Bojanowski K, Ingber DE. 1997. Mechanical continuity and reversable chromosome disassembly within intact genomes removed from living cells. J. Cell. Biochem. Submitted
49. Maniotis A, Chen C, Ingber DE. 1997. Direct evidence for mechanical connections between cell surface integrin receptors, cytoskeletal filaments and the nucleoplasm in living cells. Proc. Natt. Acad. USA. In press
50. McNamee H, Ingber D, Schwartz M. 1993. Adhesion to fibronectin stimulates inositol lipid synthesis and enhances PDGF-induced inositol lipid breakdown. J. Cell Biol. 121:673-78
51. McNamee HP, Liley HG, Ingber DE. 1996. Integrin-dependent control of inositol lipid synthesis in the focal adhesion complex. Exp. Cell Res. 224:116-22
52. Miyamoto S, Akiyama S, Yamada KM. 1995. Synergistic roles for receptor occupancy and aggregation in integrin transmembrane function. Science 267:883-85
53. Mooney D, Hansen L, Langer R, Vacanti JP, Ingber DE. 1994. Extracellular matrix controls tubulin monomer levels in hepatocytes by regulating protein turnover. Mol. Biol. Cell 5:1281-88
54. Mooney D, Langer R, Ingber DE. 1995. Cytoskeletal filament assembly and the control of cell shape and function by extracellular matrix. J. Cell Sci. 108:2311-20
55. Pienta KJ, Coffey DS. 1991. Cellular harmonic information transfer through a tissue tensegrity-matrix system. Med. Hypoth. 34:88-95
56. Pienta KJ, Getzenberg RH, Coffey DS. 1991. Cell structure and DNA organization. Crit. Rev. Eukaryot. Gene Express. 1:355-85
57. Plopper G, McNamee H, Dike L, Bojanowski K, Ingber DE. 1995. Convergence of integrin and growth factor receptor signaling pathways within the focal adhesion complex. Mol. Biol. Cell 6:1349-65
58. αs that interact with tubulin for β-adrenergic activation of adenylyl cyclase. J. Biol. Chem. 269:21748-54
59. Prasad AR, Logan SA, Nerem RM, Schwartz CJ, Sprague EA. 1993. Flow-related responses of intracellular inositol phosphate levels in cultured aortic endothelial cells. Circ. Res. 72:827-36
60. Rathke PC, Osborn M, Weber K. 1979. Immunological and ultrastructural characterization of microfilament bundles: polygonal nets and stress fibers in an established cell line. Eur. J. Cell Biol. 19:40-48
61. Resnick N, Collins T, Atkinson W, Bonthron DT, Dewey CF Jr, Gimbrone M Jr. 1993. Platelet-derived growth factor B chain promoter contains a cis-acting fluid stress-response element. Proc. Natl. Acad. Sci. USA 90:4591-95
62. Sadoshima J, Takahashi T, Jahn L, Izumo S. 1992. Roles of mechano-sensitive ion channels, cytoskeleton, and contractile activity in stretch-induced immediate-early gene expression and hypertrophy of cardiac myocytes. Proc. Natl. Acad. Sci. USA 89:9905-9
63. Sadoshima J, Xu Y, Slayter HS, Izumo S. 1993. Autocrine release of angiotensin II mediates stretch-induced hypertrophy of cardiac myocytes in vitro. Cell 75:977-84
64. Schiro JA, Chan BM, Roswit WT, Kassner PD, Pentland AP, et al. 1991. Integrin α2β1 (VLA-2) mediates reorganization and contraction of collagen matrices by human cells. Cell 67:403-10
65. Schmidt CE, Horwitz AF, Lauffenburger DA, Sheetz MP. 1993. Integrin-regulated cytoskeletal interactions in migrating fibroblasts are dynamic, asymmetric and regulated. J. Cell Biol. 123:977-91
66. Sheetz MP, Wayne DB, Pearlman AL. 1992. Extension of filopodia by motor-dependent actin assembly. Cell Motil. Cytoskelet. 22:160-69
67. Sims J, Karp S, Ingber DE. 1992. Altering the cellular mechanical force balance results in integrated changes in cell, cytoskeletal and nuclear shape. J. Cell. Sci. 103:1215-22
68. Singhvi R, Kumar A, Lopez G, Stephanopoulos GN, Wang DIC, et al. 1994. Engineering cell shape and function. Science 264:696-98
69. Stamenovic D, Fredberg J, Wang N, Butler J, Ingber D. 1996. A microstructural approach to cytoskeletal mechanics based on tensegrity. J. Theor. Biol. In press
70. Sukharev SI, Martinac B, Arshavsky VY, Kung C. 1993. Two types of mechanosensitive channels in the Escherichia coli cell envelope: solubilization and functional reconstitution. Biophys. J. 65:177-83
71. Thoumine O, Ziegler T, Girard PR, Nerem RM. 1995. Elongation of confluent endothelial cells in culture: the importance of fields of force in the associated alterations of their cytoskeletal structure. Exp. Cell Res. 219:427-41
72. Urry D. 1992. Free energy transduction in polypeptides and proteins based on inverse temperature transitions. Prog. Biophys. Mol. Biol. 57:23-57
73. Vandenburgh HH, Shansky J, Solerssi R, Chromiak J. 1995. Mechanical stimulation of skeletal muscle increases prostaglandin F2α production, cyclooxygenase activity, and cell growth by a pertussis toxin-sensitive mechanism. J. Cell. Physiol. 163:285-94
74. Wang N, Butler JP, Ingber DE. 1993. Mechanotransduction across the cell surface and through the cytoskeleton. Science 260:1124-27
75. Wang N, Ingber DE. 1994. Control of cytoskeletal mechanics by extracellular matrix, cell shape, and mechanical tension. Biophys. J. 66:2181-89
76. Wang N, Ingber DE. 1995. Probing transmembrance mechanical coupling and cytomechanics using magnetic twisting cytometry. Biochem. Cell. Biol. 73:1-9
77. Watson GM, Hessinger DA. 1992. Receptors for N-acetylated sugars may stimulate adenylate cyclase to sensitize and tune mechanoreceptors involved in triggering nematocyst discharge. Exp. Cell Res. 198:8-16
78. Wayne R, Staves MP, Leopold AC. 1992. The contribution of the extracellular matrix to gravisensing in characean cells. J. Cell Sci. 101:611-23
79. Wilson E, Sudhir K, Ives HE. 1995. Mechanical strain of rat vascular smooth muscle cells is sensed by specific extracellular matrix/integrin interactions. J. Clin. Invest. 96:2364-72
80. Yoshida M, Westlin WF, Wang N, Ingber DE, Rosenweig A, et al. 1996. Leukocyte adhesion to vascular endothelium induces E-selectin association with the actin cytoskeleton. J. Cell Biol. 133:445-55